Abstract
Life on earth is threatened both by environmental pollution and overpopulation. Natural phenomena contributing to pollution have always existed but anthropogenic activities are increasing contamination of air, soil and water. Waters are especially polluted by metals. The main threats to life from toxic metals are associated with exposure to Pb, Cd, Hg and As, which accumulate in organisms. Overpopulation means more food is required but the amount of arable land is declining due to human requirements. One way of overcoming these consequences of overpopulation is to exploit seas and oceans. Thus, the consumption of seafood has increased in recent years, especially in coastal regions. However, as many traditional fishing grounds have been over-fished, aquaculture seems a viable solution to these problems. Marine mussels are an excellent candidate for aquaculture. However mussels accumulate a wide range of metals in their soft tissue. Thus, the determination of the concentrations of potentially toxic substances in mussels is essential because of their usage as seafood and the potential adverse effects of their consumption on human health. Moreover, as contamination by metal pollutants continues and is even increasing in some parts of the world, particularly in less developed countries, it is also important to determine the level of pollution in the marine environment, especially in regions where aquaculture is foreseen and where the local population consumes large amounts of mussels.
In this review, these issues are presented and discussed using the Mediterranean mussel Mytilus galloprovincialis as an example. When this mussel is in its best condition, the meat weight can approach 50% of the total wet weight, i.e., M. galloprovincialis is very efficient at converting low value victuals into high quality animal protein. For all these reasons, M. galloprovincialis is an ideal candidate in attempts to alleviate famine through aquaculture. Mussel farming is a relatively “clean” operation because no pollutants are released into the environment. The mussels remove suspended materials from the water column, thereby improving the local water quality. However mussels accumulate metals. Metal concentrations in M. galloprovincialis are valuable indicators of contamination of coastal and estuarine ecosystems. “Mussel Watch”, introduced in 1975, is the longest continuous contaminant monitoring program of coastal waters for assessing spatial and temporal trends in coastal contamination, providing a baseline for assessing the impacts of anthropogenic and natural events and identifying contamination hot spots.
In Europe, the production of cultivated mussels is almost five times higher than wild collected mussels. Recently, the production of M. galloprovincialis in Europe has been increasing rapidly in Greece and Turkey but Spain is still the largest producer of mussels in Europe. The production of the mussel M. galloprovincialis in Spain is about 25% to the total world production, over 200,000 t y−1. Only China has a larger production of these mussels than Spain, about 600,000 t y−1. However, the bioaccumulation of toxic contaminents, mainly Cd, Pb, Hg and As, remains an issue concerning the consumption of mussels. A review of literature data revealed large variations in the Cd, Pb, Hg and As concentrations in M. galloprovincialis from their endemic areas, e.g., Mediterranean, Adriatic and Black Sea and that the concentrations of these toxic metals were generally in the following order: As > Pb > Cd > Hg. The levels of Cd, Pb and Hg were the lowest in mussels from the Aegean Sea, compared to the others investigated Seas, but a very high level of As was found.
The guidelines on the trace elements for seafood safety set by different countries and associations are reviewed. The defined legal limits on permissible concentrations of non-essential elements that are toxic in traces, such as Cd, Pb, Hg and As, in mussels on a wet weight basis in mg/kg are in the ranges: for Cd from 0.1 to 4.0; for Pb from 1.0 to 6.0; for Hg from 0.05 to 10 mg/kg and for As from 0.5 to 86 mg/kg. The reviewed Provisional Tolerable Weekly Intake values appear to support the conclusion that risk to human health from dietary exposure to the investigated elements from Mediterranean mussels is relatively low. Comparison of the published data with European legislation showed that the levels of Cd, Pb and Hg generally did not exceed the existing limits in all the mussels analyzed, excluding mussels from hot spots, such as lagoons and harbors in the Mediteranean, Adriatic and Black Sea.
Overall, the assessment that the investigated toxic elements may pose a health risk to heavy mussel consumers, especially related to the levels of Pb and Cd in M. galloprovincialis from hot spots in the all investigated Seas. Although consumption of these mussels provides proteins, essential minerals and vitamins, and thus, some protection from certain diseases, the risks and benefits of their consumption are still hard to assess because of the metals bioacumulated from the marine environment, with their reviewed toxicity. The final conclusion of this review is that M. galloprovincialis is an excellent candidate for aquaculture but that extreme care must be taken when choosing the location of farms. Care should also be taken by coastal populations when consuming wild mussels from contamination hot spots.
1 Introduction
The world population has increased almost three times in the last 60 years. The population is increasing rapidly, which means simply greater food production and more jobs are required. Although, vegetable production is enough for the present population and is likely to be for the future population, the intake of animal protein is insufficient in spite of the attempts made during the last 60 years, Culha et al. (2008).The world population is estimated to increase from about six billion currently to 8.3 billion by 2025, Bowen and Crumbley (1999). Presently, 60% of the world’s population is estimated to live in coastal areas and the present population of coastal areas exceeds the global population of just 50 years ago, Bowen and Crumbley (1999). Over two billion people worldwide rely on seafood as the major source of protein in their diet, and seafood consumption continues to increase worldwide, FAO (2006). Additionally, the sustainability of remote coastal populations depends on a source of uncontaminated seafood. Natural stocks of seafood have been supplemented by the aquaculture industry, Bowen and Crumbley (1999).
Aquaculture commenced primarily in Asia but has now spread to all continents, Subasinghe et al. (2009). From an activity that was family-based and non-commercial, aquaculture now includes large-scale commercial and industrial production of a range of high-value aquatic species that are traded at national, regional and international levels, Holmyard (1997), although production remains predominantly Asian, Subasinghe et al. (2009). Worldwide, aquaculture has shown an average annual world growth rate of 8.8% per year since 1970, which is higher than that of any other animal food-production sector Dias et al. (2009). Aquaculture plays an important role in global efforts to eliminate hunger and malnutrition by supplying aquatic products rich in protein, essential fatty acids, vitamins and minerals, Subasinghe et al. (2009). In addition, through its development, expansion and intensification, aquaculture makes significant contributions to development by improving incomes, providing employment opportunities and increasing the returns on resource use.
Mollusks are among the most successfully cultured and commercially important types of shellfish and a large variety of different mollusk species are cultured throughout the world. Seafood, notably fish, shrimp and mussels, is of value for both local consumption and export revenue, Culha et al. (2008). In recent years, the consumption of seafood has increased, Kalogeropoulos et al. (2004), Perugini et al. (2007) and marine mussels are commercially important seafood species worldwide, Phillips (1980), Widdows (1985), Farrington et al. (1987), Holmyard (1997), Prou and Goulletquer (2002), Smaal (2002), Nesto et al. (2007), Culha et al. (2008) and their production is increasing worldwide, FAO (2006). Mussel (Mytilus spp.) production is one of the most economically important aspects of global aquaculture. The farming of mussel (Mytilus spp.) is without doubt the most efficient way to convert the organic matter produced by marine organisms in the first link of the food chain, phytoplankton and the remains thereof, into palatable and nutritious human food, Culha et al. (2008). According to data from 2002, the annual world production of mussels Mytilus galloprovincialis was 1.690.835 t, Ozden et al. (2010). In Europe, production is known to consist of M. galloprovincialis, M. edulis and a third, less profitable species M. trossulus, but only in the Baltic Sea, Dias et al. (2009). Mussels are important for the mariculture industry in Europe and the annual production exceeds 800,000 t, Smaal (2002).
The Mediterranean mussel, M. galloprovincialis, is endemic to the Mediterranean, Black and Adriatic Sea and the Atlantic Ocean from Ireland to Morocco, Gosling (1992). The mussel species M. galloprovincialis is raised mainly in the Mediterranean and farming of this species is common along the coastlines of a number of countries in the region: France, Spain, Italy, Sicily, Greece and Tunisia, Smaal (2002). The culture of M. galloprovincialis in the Black Sea region has recently been developing but is not yet widespread. However, there are mussel farms in the Marmara and Aegean Sea in Turkey, Karayücel et al. (2010).
The Mediterranean mussel is an invasive, warm-water species frequently transported by human activities. It is highly invasive where it has been introduced, including in Australia, Asia, California and the Puget Sound in the United States, Gosling (1992), Geller et al. (1994) and Anderson et al. (2002). This species has also been successfully introduced in South Africa, where it now dominates over other locally farmed species, Gangnery et al. (2004).
Mussel farming is a relatively “clean” operation. As filter feeders, mussels tend to remove suspended materials from the water column, thereby improving the local water quality. Regardless of the technology employed, the culturing of mussels does not involve the application of feed or the release of pollutants in any other way. M. galloprovincialis is a filter feeding animal, which depends on phytoplankton, organic detritus, bacteria and, probably, dissolved organic matter in the water as sources of food. It is well-known that through feeding, mussels accumulate a wide range of metals from water. Metal concentrations in the mussel M. galloprovincialis can provide a measure of the effects of potential pollutants in marine environments, Goldberg and Bertine (2000), Pergent-Martini and Pergent (2000), Romeo et al. (2003a, b, 2005), Morillo et al. (2005), Usero et al. (2005), Gorbi et al. (2008), Deudero et al. (2009), Stankovic et al. (2005, 2006, 2008), Fernández et al. (2010), Bartolomé et al. (2010b), Jovic et al. (2011), and information of direct ecological significance, Costas-Rodríguez et al. (2010), Tsangaris, et al. (2010) and potential relevance to human health, Culha et al. (2008). Seafood is a major source of animal protein and very rich sources of mineral components, Fuentes et al. (2009), Ozden et al. (2010).The health benefits associated with the consumption of seafood products are particularly important for the prevention of heart-related diseases and for many vulnerable groups, such as pregnant and lactating women, infants and children, Cozzolino et al. (2001), Christophoridis et al. (2009).
The distribution of metals within aquatic environments is governed by complex processes of material exchange affected by various anthropogenic activities or natural processes, including reverine or atmospheric inputs, coastal and seafloor erosion, biological activities, water drainage and discharge of urban and industrial wastewaters. The sources of pollutant metals in the marine environment are mainly from industrial processes and discharge of metal-containing waste, landfill leachates and secondary precipitation of polluted airborne matter. As pollutant metals are widely distributed in coastal environments, due to both natural geological processes and anthropogenic activities, the determination of the level of potentially toxic substances in mussels is important because of their negative effect on human health, Giusti and Zhang (2002), Kwoczek et al. (2006), Sivaperumal et al. (2007), Kayhan et al. (2007), Turkmen and Ciminli (2007), Çevik et al. (2008), Baeyens et al. (2009), Ozden et al. (2010).
Mussels have proven themselves to be useful for biomonitoring chemical contamination and, therefore, have been used for indicating levels of trace metal concentrations in the marine environment, Conti and Cecchetti (2003). Mussels of the genus Mytilus have been employed extensively in Mussels Watch Programs to establish current trace metal levels in coastal environments, e.g., in the USA, the UK, Australia, Hong Kong and France, Przytarska et al. (2010). Mussels Watch Programs are considered efficient tools to study environmental trace metal levels and they have been adopted in many countries, Hellou and Law (2003). To safeguard public health, maximum acceptable concentrations of toxic contaminants have been established in various countries. Thus, in the framework of numerous legislative measures, many monitoring programs have been performed to investigate the health quality of marine species used as human seafood, including mollusks, in European and Asian regions, Franco et al. (2002), Marcotrigiano and Storelli (2003), Liang et al. (2004), Yap et al. (2004), Kwoczek et al. (2006), Kljakovic-Gaspic et al. (2007), Marti-Cid et al. (2007), Nesto et al. (2007), Sivaperumal et al. (2007), Amirad et al. (2008), Sloth and Julshaman (2008), Metain et al. (2009), Whyte et al. (2009), Jovic et al. (2009, 2010), Ozden et al. (2010), Dahl et al. (2010). Thus, balancing the risks and benefits of seafood consumption is clearly a topic of interest. Much has been realized in the case of fish, Gochfeld and Burger (2005), but risk assessment is not so well developed in the case of shellfish, Amiard et al. (2008).
The interactions between the seas and human health are increasing, in part, due to the increasing numbers of humans living within close proximity of the world’s seas. The consequences of this are: higher usage of sea resources as food and the greater possibility of contamination of the coasts. The necessity for monitoring metal pollution of coastal waters is therefore important worldwide from the commercial and resource sustainability points of view.
2 Mediterranean Mussel – Mytilus galloprovincialis
2.1 Distribution
Three Mytilus mussel taxa are present in European coastal sea waters: Mytilus galloprovincialis (Mediterranean mussel), Mytilus edulis (Blue mussel), and Mytilus trossulus (Baltic mussel), Gosling (1992), Śmietanka et al. (2004). The Mediterranean mussel M. galloprovincialis is a temperate, warm-water mussel, occurring in more exposed locations which do not experience pronounced salinity variations and also in southern areas such as the Black Sea, the Mediterranean and the Iberian Atlantic coast. M. edulis is a temperate, cold-water mussel, which can live in brackish water and predominates in central and northern Europe. M. trossulus, a cold-water species that can tolerate low salinities, occurs in the Baltic Sea and presumably some areas in northern Europe, Kijewski et al. (2009).
The Mediterranean mussel, M. galloprovincialis, is endemic to the Mediterranean Sea, the Adriatic Sea and the Atlantic Ocean from Ireland to Morocco, Gosling (1992). Due in part to its capacity to tolerate warm-water conditions, the Mediterranean mussel is a warm-water invasive species, Branch and Steffani (2004), frequently transported by human activities, Geller et al.(1994), Anderson et al. (2002). From its source in the Mediterranean, M. galloprovincialis has colonized the sea waters of Hong Kong, Japan, Korea, southeast Australia, Hawaii, Mexico, California, the west and east coast of Canada and perhaps Britain and Ireland and arrived accidentally in South Africa in the mid-1970s, Branch and Steffani (2004), since when its geographic range has extended at about 115 km year−1, Kijewski et al. (2009). It is not known whether the expansion of its range in the Atlantic and Pacific Oceans is due to climate change or human activity but is probably a mixture of the both, Braby and Somero (2006), Coghlan and Gosling (2007) Wonham (2004), Zardi et al. (2007).
It is known that M. galloprovincialis is able to out compete and displace native mussels and has become the dominant mussel species in certain localities. This was case with the native mussel Perna, Branch and Stephanni (2004). This is because M. galloprovincialis may grow faster than native mussels, be more tolerant to air exposure and have a reproductive output of between 20% and 200% greater than that of indigenous species, Branch and Stephanni (2004). Thus, M. galloprovincialis is both ecologically invasive and a source of ‘genetic pollution’ that may threaten the genetic integrity of a native mussel species over much of its geographic range, Hilbish et al. (2010).
M. galloprovincialis, M. edulis and M. trossulus are closely related species, the identification of which has long been controversial. More accurate species identification is now possible using genetic methods, Inoue et al. (1995), Gosling et al. (2008), Dias et al. (2009). The three species are known to hybridize wherever their geographic ranges overlap, Zardi et al. (2007), Dias et al. (2009). Well-studied hybrid zones of M. galloprovincialis include the areas between southwest France and the Scottish coasts between M. galloprovincialis and M. edulis, Skibinski et al. (1983), Gosling (1992) and Hilbish et al. (2002); on the west coasts of North America between M. trossulus, M. galloprovincialis and M. edulis, Braby and Somero (2006), Johnson and Geller (2006) Shields et al. (2008). There remains debate about the true taxonomic status of these two “species” because wherever their distributions overlap they can hybridize and their hybrids are fertile, Dias et al. (2009). Its occurrence in Britain and Ireland is still an open question: whether its occurrence there due to introduction or is simply an expansion of its natural range in the Mediterranean, Branch and Steffani (2004). In Scotland, small numbers of M. galloprovincialis and its possible hybrids were identified, M. trossulus (37%) was found to be more common than M. edulis (30%) and 23% of the sampled mussels were M. trossulus and M. edulis hybrids, Dias et al. (2009). Identification of M. galloprovincialis and M. edulis (and any hybrids) based on shell shape is usually uncertain because of the extreme plasticity of shape exhibited by the mussels under environmental variation. Since 1995, a DNA-based genetic method that seems truly diagnostic for European populations of these species has become available, Inoue et al. (1995) and Wood et al. (2003).
However, no large scale studies have yet been carried out to characterize the mosaic of populations of Mytilus spp. and their hybrids. Up to the early 1990s, all mussels from Western Europe were considered to be M. edulis. Now, it is known that the mussels from southern Brittany (France) to the Mediterranean Sea are M. galloprovincialis. The knowledge of the distribution of mussel species around Europe, as was assessed in 1992, is given in Fig. 9.1, Gosling (1992).
Approximate distributions of M. galloprovincialis, M. edulis and M. trossulus in Europe, Gosling (1992). It would appear that M. galloprovincialis prefers slightly warmer water than the other two European Mytilus species but, due to its invasive nature, has spread from the Mediteranean region to the slightly warmer waters of northern Europe
2.2 Biology
M. galloprovincialis is an endemic Mediterranean species, the exact distribution range of which is not well defined due to the confusion with the very similar congener M. edulis. The Mediterranean mussel M. galloprovincialis is known from classical texts of Greek antiquity and their use in diet and medicine by humans in the Mediterranean coastal areas, Voultsiadou et al. (2010 ) . It is dark blue or brown to almost black, Fig. 9.2. The two shells are equal in size and nearly quadratic. The outside is black-violet colored; on one side the rim of the shell ends with a pointed and slightly bent umbo, while the other side is rounded, although the shell shape varies by region.
The Mediterranean mussel M. galloprovincialis
In its native range, M. galloprovincialis can be found from exposed rocky outer coasts to sandy bottoms. It is an intertidal species extending down to a depth of 40 m and it may be found on all European coasts with hard substrata. It lives attached by byssus threads to rocks, piers and ropes within sheltered embayment, harbors, estuaries and on open rocky shores, while it may also form dense mussel beds directly on sandy-muddy bottoms in favorable sites. Unlike the other 26 Asian and Atlantic mollusks introduced into Pacific regions, only the Mediterranean mussel as an introduced species occurs on open coasts; all the remaining species are restricted to bays and estuaries, Carlton (1992). The invaders typically require rocky coastlines with a high rate of water flow.
The Mediterranean mussel tends to grow larger than its cousins, up to 15 cm, although typically only 5–8 cm. Intertidal specimens often remain small, rarely exceeding 6 cm, while deep-water individuals often attain a length of 9 cm and occasionally may even reach 15 cm. A 5 cm-long mussel can filter 5 l water/h. While mussels grow to optimum size in sea water of temperature 15–25°C, their biological activities are decreased over 25°C. They are resistant to 5–40% salinity, but the optimal degree of salinity is between 20% and 35%, Braby and Somero (2006). The continuous upwelling of cold nutrient-rich water during heavy rains probably stimulates an abundance of phytoplankton. The mean density in the most crowded beds may reach 24,000 mussels/m², Voultsiadou et al. (2010). Greece together with Italy and Spain are the Mediterranean countries with the largest catches of M. galloprovincialis FAO (2007).
Mussels are bivalve mollusks and much is known of their biology mainly because they have been an easy marine organism to collect and study, Gosling (1992). The two shells are equal in size and nearly quadratic. The outside is black-violet colored; on one side the rim of the shell ends with a pointed and slightly bent umbo, while the other side is rounded, although the shell shape varies by region. The two valves of the shell are held tightly closed by a large posterior adductor muscle when the mussel is exposed to air. Feeding and respiration are realized via currents of water directed across the gills. Digestion occurs in the digestion gland, brown-greenish in color, situated in the centre of the body. Mussels feed on phytoplankton and organic matter. Food particles are trapped by cilia on the gills and carried in mucous strings to the mouth, but this is a selective process and some particles are rejected before entering the gut, Beaumont et al. (2007).
Mussels can move with the aid of a foot. The foot of a mussel is an important organ because it enables the mussel to attach itself by byssus threads to a solid substrate. The threads can be broken and replaced at will, allowing mussels to re-orientate themselves within clumps or in rock cracks or crevices. Byssal attachment is an important, sometimes critical, factor in mussel aquaculture, Beaumont et al. (2007).
The reproductive cycle of M. galloprovincialis varies greatly according to geographic region and is characterized by one or two major spawning events per year and a more or less long resting period after spawning events, Gangnery et al. (2004). Maturation of eggs and sperm occurs in the gonad tissue that develops within the folds of the mantle and, depending on environmental temperature and food availability, mussels may spawn just once or several times each year, Beaumont et al. (2007). In Galicia, Spain, M. galloprovincialis reproduction may occur at any time of the year. The two main reproductive peaks of the year are in spring and autumn. Immediately after the reproduction process, a mussel can lose up to 70% of its soft tissue, Cossa (1989). The sexes are separate in mussels, but there are no morphological differences between males and females. Even in ripe mussels where the mantle is packed with gametes, eggs or sperm, the mantle color is not always a reliable guide to the sex of an individual because the eggs can range in color from white to orange/pink. Two days after fertilization, the embryos develop into planktonic larvae that are dispersed by sea and ocean currents, Beaumont et al. (2007). The larvae settle after 4–8 weeks at a size of 250–300 microns shell length and may have a secondary post-larval dispersal phase by “byssus drifts” up to a size of 2 mm shell length Beaumont et al. (2007). Due to their high fecundity, their extensive larval and post-larval dispersal capability, their ability to attach by byssus threads to non-specific substrates and also to one another and their fast growth, mussels are often a very significant and abundant element of the ecology of many inter-tidal and sub-tidal habitats, Gosling (1992).
Factors such as water temperature, nutrient availability and the reproduction cycle of mussels can influence meat yield, microbiological characteristics and biochemical composition of these mussels, Vernocchi et al. (2007). The overall quality of mussels is the result of biological, chemical and organoleptic characteristics, such as the aspect of the shells, meat aspect and yield, typical taste and flavor, Vernocchi et al. (2007). Meat weights can approach 50% of the total wet weight when the mussels are in their best condition. When a large percentage of the mussels are close to spawning or just past spawning, harvesting should be postponed until they are in better condition. Production extends over 17–18 months for seeding in summer and over 22 months for seeding in mid-winter, Gangnery et al. (2004).
2.3 Ecology
Measuring and monitoring pollutant levels in organisms, i.e., bio-monitoring these levels, represents the only method that takes into account and integrates all the changes in the water quality which may influence the accumulation of pollutants in seafood and, ultimately, their possible transfer to mankind via seafood consumption, Rodriguez y Baena and Thébault (2006). Mussel Watch programs have been used to assess coastal environmental pollution as a framework to put national data into a global context. Therefore, monitoring programs were historically conceived to control the quality of the marine environment without special emphasis on how contamination of the media could potentially impact the health of edible organisms and mankind. Most of the reports were based on quantifying contamination, but some of the oldest were on the nutritional use of oysters in the treatment of anemia. Results for the trace elements Cr, Ni, Cu, Zn, As, Se, Ag, Cd, Sn, Sb, Hg, Ti, and Pb in mussels and oysters were entered into four files to create the World Mussel Watch data base.
However, during the past few decades there has been increasing evidence of the existence of a deep, mutual relationship between the health of the environment and that of mankind. Strict environmental monitoring activities have thus adopted an ecosystem-based approach, and Mussel Watch programs have been developed following this innovative concept. Nowadays, WMW data are results from two long-term Mussel Watch Programs: the Reseau National d’Observation de la Qualite du Mulieu – Marin Mussel Watch in France and National Status and Trends – Program in the United States, Cantillo (1998).
The first Mussel Watch program was implemented in the USA during the mid 1970s by Goldberg (1975) in order to monitor levels of pollutant trace elements and organochlorines, and more recently those of several biochemical parameters in marine coastal waters. The US Mussel Watch is coordinated by the National Oceanic and Atmospheric Administration and was extended to Latin America in the early ’90s. The bivalve species used to biomonitor these regions are the blue mussel M. edulis and the Californian mussel M. californianus along the North Atlantic and the Pacific coasts, and the American oyster Crassostrea virginica in the Gulf of Mexico and Southern Atlantic, Cantillo (1998).
Several European countries have implemented similar national Mussel Watch programs, e.g. France, Italy and Spain. For instance, in France the French Research Institute for Exploitation of the Sea developed the “Réseau National d’Observation” in 1974 to assess the levels of metals and organochlorines along the French coastlines. Biota, the mussels M. edulis and M. galloprovincialis and the oyster C. gigas, are collected twice a year at about 100 sampling sites, passive biomonitoring in the RNO program. In the second phase, the “Réseau Intégrateur Biologique” was implemented in 1996 to monitor the concentrations of chemicals and radiochemicals in organisms caged for several weeks prior to collection, active biomonitoring by the RINBIO program, Andral et al. (2004). Despite the presence of several ongoing national programs, no large-scale Mussel Watch network was coordinated at the Mediterranean level until 2002, when the “Commission Internationale pour l’Exploration Scientifique de la Mer Mediterranee” launched a program called the Mediterranean Mussel Watch, designing a regional program for the detection of radionuclides and trace contaminants in sentinel organisms. The CIESM developed and implemented a regional MMW program using the mussel M. galloprovincialis as the bioindicator species to document reliable baseline levels of radionuclides and pollutant metals in the coastal waters of the Mediterranean and Black Sea, Rodriguez y Baena and Thébault (2006).
Ever since Goldberg et al. (1978) proposed the application of the ‘Mussel Watch’ concept, based on the suitability of mussels as bio indicators of contamination, most national and international monitoring programs of marine pollution have adopted this concept and the MMW started with limited sampling sites in each country, Sunlu (2006), Catsiki and Florou (2006). For example, studies of trace metal levels in M. galloprovincialis from Turkish sea coasts have been comparatively few and little data has been published in the scientific literature, Sunlu (2006).
International monitoring programs have established some standards for sampling and sample preparation procedures to reduce sources of variation, other than the metal content itself, in the contamination levels in mussels. These include, among others, sampling depth and season and the size of the individuals. Mussels are known to have a high capacity for metal accumulation, as reported in various mussel watch programs, Goldberg et al. (1978), making them potentially very dangerous for consumers. Therefore, strict metal controls are required in order to guarantee the safety of the product. The potential hazard of metals has long been recognized.
3 Mediterranean Mussel as a Seafood
3.1 World Mussel Production
The population is increasing rapidly, which means simply more food production and more jobs are required. Although, vegetable production is sufficient for the present population and is likely to be for the future population, the intake of animal protein is inadequate in spite of attempts made during the last 60 years. This gap has not yet been closed. For this reason, the world aquaculture production has grown tremendously over the past 50 years from a production of less than one million tonnes in the early 1950s to 48.1 million tonnes in 2005, an average annual growth rate of 8.8% (Fig. 9.3a,b), Subasinghe et al. (2009). Of this production, 32.4 million tonnes (or 67.3%) was produced in China and 22.3% in the rest of the Asia–Pacific region. Western Europe contributed 4.2% with 2.0 million tonnes, while Central and Eastern Europe contributed 270 000 t or 0.6%. Latin America and the Caribbean, and North America contributed 2.9% and 1.3%, respectively. Finally, production from the Near East and North Africa, accounted for 1.2% and 0.2%, respectively, of the global total for 2005, Subasinghe et al. (2009).
(a) Contribution to seafood supply: aquacultured – light gray; captured – dark gray. In the last 40 years, the world production of aquacultured mussels has increased and nowadays aquacultured mussel production is almost double that of wild harvested mussels. (b) The world aquacultured seafood production has grown tremendously over the past 40 years. Mussel production was less than 10% of the total seefood production in the early 1970s but attained 45% in 2005, with an average annual growth rate of 8.8%
In the recent years, the consumption of seafood has increased, Perugini et al. (2007), Kalogeropoulos et al. (2004), and marine mussels are a commercially important seafood product worldwide Phillips (1980), Farrington et al. (1987), Widdows (1985). The world production of mussels, including both, aquaculture and wild harvest production, is given in Fig. 9.4, FAO (2006).
Share of world production of mussels of all species, including both aquacultured and wild harvested production. The area of the world with the largest mussel production is China. Denmark is the only country that still harvests very large quantities of wild mussels. The shares are calculated as the average for each country during 1997–2001, FAO (2006)
The area of the world with the highest mussel’s production is China. Denmark is the only country that still produces very large quantities of wild harvest mussels, but producers there are now investing seriously in increasing the capacity to culture mussels. Spain and Denmark lead the world in the production of canned products, FAO (2006).
In the last several decades, producers have been switching away from wild harvests toward a variety of culturing techniques. Hickman (1998) refers to marine mussels as an “ideal candidate for aquaculture,” having characteristics such as rapid growth rates, high productivity on almost any substrate, relatively straightforward husbandry and ability to filter plankton and take up nutrients, and resilience to disease. Most of the world’s production of mussels is canned, nearly 65%, or frozen nearly 35%; most international trade in the residual (<1%) is of high-valued premium fresh or chilled products, FAO (2006). European Union shellfish sanitation regulations limit imports of the fresh product from extra-EU sources; however, much of the international trade in fresh mussels occurs among EU countries. The Netherlands leads among the producers of fresh or chilled products for the European market.
3.2 Mytilus galloprovincialis Production
The Mediterranean mussel M. galloprovincialis is mainly cultured in coastal waters from NW Spain to the northern shores of the Mediterranean Sea. The production of this mussel has also been reported from some southern Mediterranean countries, the Russian Federation, Ukraine, South Africa and also China, Lutz et al. (1991), Gosling (2003).
Cultured and harvested mussels date back to historic times in many countries, such as in Italy >2,000 years ago, France >700 years ago and the Netherlands >100 years ago. In Spain, mussel harvesting was already described in 400 BC, but the actual Galician raft culture emerged only after 1945. Mediterranean mussel culture is now developing in Greece and Turkey, although the main yields are still produced in the traditional areas, Smaal (2002).
The exploitation of mussels as a food source in Europe consists of M. edulis, along the Atlantic and North Sea coasts and M. galloprovincialis in the Mediterranean, Adriatic and Black Sea, and in the Rias, Northwest Spain, (Fig. 9.1). Mussels are important for the mariculture industry in Europe and annual production exceeds 800,000 t and Europe produces around 50% of the annual world production of mussels, consisting of M. galloprovincialis and M. edulis, Smaal (2002). Most of the current production in Europe originates from the historically large producers: Spain, France and the Netherlands, followed by a marked increase in production in the UK, Ireland and Norway, Smaal (2002).
M. galloprovincialis and M. edulis are the most important mussel production species in Europe and the total European tonnage for the culture and capture of these two kinds of mussels from 1950 to 2004 are given in Fig. 9.5. It should be noted that the statistics provided by FAO (2006) treat mussels from the Atlantic coast of Spain as M. edulis, but, as the distribution map shows in Fig. 9.1, the species in this region is M. galloprovincialis.
Total mussel tonnage in Europe: aquaculture and capture, 1950–2004, FAO (2006). In Europe, the production of cultivated mussels in the last 20 years is more than five times higher than that of wild harvested mussels. In 2007, 52% of the EU aquaculture production was primarily mussels and oysters, but the contribution of European countries to the total world production of mussels has decreased
European aquaculture of mussels relies on natural spatfall and there are three main methods of culturing these spat up to market size: bottom cultivation, bouchot culture and the suspended rope method, Spencer (2002). Spain is by far the greatest producer of mussels by aquaculture in Europe; greater than the combined total of the other important mussel producing countries, such as the Netherlands, France, Italy, Ireland and the UK, FAO (2006). The production of the mussel M. galloprovincialis in Galicia (Northwest of Spain) contributes approximately 25% to the total world production (over 200,000 t y−1); only China has a greater production (about 600,000 t y−1), Costas-Rodríguez et al. (2010).
European countries produced 38% of the world production of mussels in 2003, FAO (2006). In 2007, 52% of the EU aquaculture production was primarily mussels and oysters and 48% of fish species. Mussel farming has an important economic impact in many European countries. The main yields of Atlantic mussels are from Spain, while the Mediterranean production predominantly comes from Italy. In Spain, mussel is the principal seafood product, while in Italy this mussel is harvested in an amount higher than 170,000 t, which represents more than 75% of the total shellfish production in Italy, Vernocchi et al. (2007).
Mussel production in France involves the two common species: M. edulis is widely distributed along the English Channel to the southwest coastline of France and M. galloprovincialis is mainly distributed on the Mediterranean shores. M. galloprovincialis has been cultivated since 1925 in French Mediterranean lagoons. The French mussel industry produces around 60,000 t on a yearly basis, with 13% from Mediterranean coast, Prou and Goulletquer (2002). Although a public mussel fishery still exists in France, most of the production is based upon 3 culture techniques: the bouchot-type culture, developed in the thirteenth century; on-bottom culture, a traditional activity, and harvests from longline culture, which have significantly increased in the last 10 years.
European aquaculture of mussels relies on natural spatfall and these three main methods of culturing the spat up to market size: bottom cultivation, bouchot culture and the suspended rope method Spencer (2002).This last technique allows development offshore, far away from any pollutant source, Prou and Goulletquer (2002).
Mussel production in these traditional areas of Europe has been stabile since the 1970s, but the contribution of European countries to the total world production has decreased due to increased production outside Europe. In these traditional mussel culture areas, new functions have developed, such as recreation and nature conservation, and therefore extension of mussel culture is now also space limited, Smaal (2002). Expansion of M. galloprovincialis mariculture in the Mediterranean occurs in areas of Greece and Turkey, i.e. in areas of the Aegean Sea, and also Marmara and the Black Sea, Karayucel et al. (2010).
Marine aquaculture in Greece is now well-established and Greek production from intensive mariculture represents almost 47% of the total intensive mariculture in the eastern Mediterranean region; the production increased from 5,800 t in 1990 to 28,100 t in the year 2000, UNEP/MAP/MED POL (2004). The North Aegean Sea is one of the most significant areas in the eastern Mediterranean Sea for bivalve production concerning both fishing and culture activities. More than 80% of the total Hellenic M. galloprovincialis production is derived from this area, Kalaitzi et al. (2007). Mussel farming is one of the most dynamic sectors of Hellenic aquaculture and the number of mussel farms in Greece has increased rapidly from five in 1980 to more than 550 in 2005, Voultsiadou et al. (2010). In Turkey, the total aquaculture production reached 139,873 t in 2007, while M. galloprovincialis culture was only 1,100 or 5,000 t, depending on the published data, Karayucel et al. (2010) or Ozden et al. (2010). The culture of M. galloprovincialis in the south region of the Black Sea is a relatively recent development and not yet widespread, but prospects for mussel culture in the Black Sea are quite high due to the favorable salinity, temperature, topography, food availability and socio-economic conditions in the area, Karayucel et al. (2010).
Mussels produced in Europe are predominantly consumed within Europe, and the major internal trade occurs between neighboring countries, Smaal (2002). Mussel markets are changing. For example in Spain, at the beginning of mussel farming, the national consumption was limited but has now exceeded 100,000 t annually, mainly as fresh mussels. The distribution of mussels was approximately 40% for the fresh market, 50% for canning and 10% for freezing. In the past decade, about 60% of the mussels were for the fresh market and 40% for canning. Exports are mainly to Italy, France and Germany.
3.3 Regulations
The oceans and seas are prime sources of food for mankind. Contamination of seafood by toxic contaminants represents a serious threat to human health and is a major economic concern. In order to protect the health of seafood consumers, many countries have set guidelines for the maximum permissible levels of toxic pollutants in seafood, EC (2006). Although such guidelines are essential for public health protection, problems can arise when guidelines are not met, which may lead to dramatic economic impacts on people and companies making their living out of sea resources. It is therefore of prime importance to monitor the levels of key contaminants in the coastal zone, where most fishery and farming activities are realized.
Most European countries have environmental quality standards, EQS, for marine aquaculture, mainly in relation to water quality and nutrient output and in the most European countries, marine aquaculture is monitored but the type and extent of seafood monitoring varies from country to country, Smaal (2002). Mussel culture is regulated by EU directives with regard to quality for the consumer in terms of pathogenic bacteria, biotoxins and chemical contaminants. The water quality of shellfish culture areas is under EU regulation: contaminant levels, EU directive 79/923/EEC; biotoxins and pathogenic bacteria, EU directive 91/492/EEC. In all European production areas, there are EU and national standards for product quality and for the environment where seafood is cultured or fished, Smaal (2002) and Prou and Goulletquer (2002). The sanitary quality and level of contaminants are monitored according to national rules, based on EU directives, but not in all countries. EU classifications of shellfish harvesting areas are given by the Shellfish Hygiene Directive 91/492/EEC. Different countries and world associations defined legal limits on permissible concentrations of non-essential elements that are toxic in traces, such as Cd, Pb, Hg and As in mussels, on a dry or wet weight basis, the values of which are given in Table 9.1.
The control of hazards for mussels is conducted according to the relevant EU legislation (EU Directive 1881/2006 – EC (2006)). The controls include parameters such as marine biotoxins, microbiological indicators, radionuclides, organohalogenated substances and pollutant metals. It should also be emphasized that every movement of mussels (for processing or sale) requires the approval of a Competent Veterinary authority, which takes into account the analysis results of the above-mentioned parameters. This approval is recorded on the mussel registration forms, which are actually the “passport” of mussels for their marketing.
In the near future, the mussel industry will face several challenges since it might be less costly than other protein products and a comparative evaluation of the environmental costs could be useful for making decisions on the development options and improved management, including all necessary regulations, such as increased sanitary regulations too, Prou and Goulletquer (2002). This could result in further off-shore development of mussel cultures, which might lead to space conflicts with other users, such as tourism and fisheries, Smaal (2002), Prou and Goulletquer (2002).
4 Pollutant Trace Elements
Metals toxic in the trace have been used by humans for thousands of years. They are natural components of the earth’s crust and cannot be destroyed. Although there are many elements that are classified as metals toxic in the trace, the ones of most concern, with respect to their biotoxic effects and presence in food are Cd, Pb, Hg and inorganic As. These metals are very toxic and their absorption and toxicity depends on dose and, among other diet constituents, on the intake of essential metals through diet. These elements have no known bio-importance in human biochemistry and physiology and their consumption, even at very low concentrations, can cause toxic effects, because they tend to accumulate in the human body over time. The major routes of exposure of the general population to Pb, Cd, Hg and As are through air, water and diet Järup (2003).
Pollutant trace elements can be present in food either naturally or as a result of human activities, such as mining, irrigation, energy extraction, agricultural practices, incineration, industrial emissions and car exhausts. The contamination chain of pollutant trace elements almost always follows the cyclic order: industry, atmosphere, soil, water, fish, and humans, Suseno et al. (2010). Pollutant trace elements have the ability to bioconcentrate in organisms directly from the water, bioaccumulate and biomagnify in the food chain, causing higher trophic organisms to become contaminated with high concentrations of chemical contaminants, Suseno et al. (2010). They tend to undergo interactions and transformation in sea water, sediments and marine biota, due to physical, chemical, microbial or light-mediated mechanisms. The variability of metal concentrations in marine organisms depends on many factors, either environmental, such as metal concentrations in sea water, temperature, salinity, dissolved oxygen, pH or purely biological i.e., species, tissues, organs, feeding conditions, Sunlu (2006). They may also originate from contamination during manufacture, processing and storage, or from direct addition. They are stable elements and persist for long periods in the environment. There is evidence to suggest that the levels of As and Cd in mussels are decreased by processing or freezing, Devesa et al. (2008), Dahl et al. (2010) and Metian et al. (2009), and Cd and Pb are increased by canned storage, Waheed et al. (2003). However, for example, methyl mercury, Me-Hg, can be found in canned fish that has undergone severe thermal treatment, Lawley et al. (2008).
Bioaccumulation phenomena in marine organisms may result from food-chain biomagnification processes or from concentration of pollutants by filter feeders. Metal concentrations in the mussels M. galloprovincialis are used as an indicator of marine pollution. In addition, toxic metals may be accumulated in marine organisms up to levels which may affect the mussels directly, e.g., by killing their larvae or damaging shell growth, thus affecting their quantity and quality. Moreover, because the pollutant trace elements are potentially detrimental to human health, their presence can limit the quantity of mussels humans can consume, Andersen et al. (1996).
4.2 Properties and Sources of the Toxic Elements
Metals fall into one of two categories, essential and non-essential. Essential metal micronutrients, such as Cu, Zn, Fe, Mn, Co, Cr and Se, are required in small quantities, a few mg or μg per day, for the optimal functioning of biological and biochemical processes in humans, Verplanck (2003). Essential metal micronutrients, such as Ca, Mg, Na, P and S, are also required for similar biochemical processes, but in larger quantities, 100 mg or more per day, Verplanck (2003). Non-essential elements, such as Cd, Pb, Hg and As, have no known biological function in organisms and exert their toxicity by competing with essential metals for active enzyme or membrane protein sites. Moreover, Mytilus species are able to synthesize the metal-binding protein, metallothionein, for metal detoxification, Kohler and Riisgard (1982).
Regardless of the class of a metal, it is the dose that makes a poison. Exposure to either an excess or deficient amount of metal causes various toxic effects within an organism. These effects vary, depending upon whether the exposure is chronic or acute, and whether they are mutagenic, carcinogenic or teratogenic, developmental defects, in nature. In general, pollutant metals produce their toxicity by forming complexes or ligands with organic compounds. Such modified biological molecules lose their ability to function properly and can result in malfunctioning or death of the affected cells. The most usual elements involved in ligand formation are oxygen, sulfur and nitrogen, Merian (1991). The following sections contain information on the mode of action and routes of uptake and elimination of the four pollutant metals present in this mussel: Cd, Pb, Hg and As.
4.2.1 Cadmium (Cd)
Cd is non-essential element commonly used in the electroplating industry, as a paint stabilizer, color pigment fixer in plastics and in agriculture fertilizers. In non-polluted freshwaters, it has a concentration lower than 1 μg/L while in seawater the concentration ranges from 0.04 to 3.0 μg/L, Chang (1996).
Cereals, fruit and vegetables are the main source of Cd in the diet, making up about 66% of the mean Cd intake. The other sources include meat and fish, with liver, kidney, crustaceans, mollusks and cephalopods containing comparatively higher Cd levels. The main routes of aqueous Cd uptake in aquatic organisms are via the gills or gut; subsequently, it binds to low molecular weight proteins metal-lothioneins and accumulates in the liver and kidneys, making Cd difficult to extract, Widmeyer et al. (2004).
4.2.2 Lead (Pb)
Pb is a non-essential element commonly used by the battery industry, as a gasoline additive, and in the pigment/paint and metal alloy industries. The concentrations in freshwater vary considerably with values ranging from 34 to 300 μg/L, while in seawater they range from 0.3 to 20 μg/L, Chang (1996). None of the most commonly consumed foods were found to be high in Pb. The most common uptake routes are via the lungs or gills, as it is not commonly absorbed by the tract/gut. The general population is exposed to Pb through food, water and air. Exposure to Pb from the air is higher in the urban population. Hazards from these sources have gradually diminished due to the exclusion of Pb from gasoline. Absorption of Pb from ingested food and water greatly depends on the levels of other element present in the diet, such as calcium, iron, and zinc. It was shown that dietary deficiencies in these essential elements enhance Pb absorption, Goyer (1995).
4.2.3 Mercury (Hg)
Elemental Hg naturally occurs in lakes and streams, but emissions from industrial and mining processes and the burning of fossil fuels concentrate elemental Hg in the environment. The form of Hg hazardous in drinking water is the inorganic form, which can easily be converted to the organic Me-Hg form by the action of bacteria present in marine and freshwater sediments. It is this form that eventually enters the food chain, Selin (2009). In non-polluted freshwaters, it has a concentration lower than 1 μg/L, while in seawater the concentration is lower than 4 μg/L, Fitzgerald and Clarkson (1991). Once in the environment, microorganisms within the lakes and streams convert elemental Hg to Me-Hg, which travels from the oceans to phytoplankton and seafood. However, the study of Me-Hg uptake by phytoplankton and its transfer through the various components of trophic webs is a challenging issue for a better understanding of its bioaccumulation and biomagnification processes in marine seafood.
The main source of Hg in the diet is fish. Fruit, dried fruit, mushrooms and vegetables are other sources of Hg. Hg accumulated in the tissues of seafood usually takes the form of Me-Hg, which is largely responsible for the accumulation of Hg in organisms i.e., bioaccumulations, and the transfer of Hg from one trophic level to another i.e., biomagnifications. Bioaccumulated organic Hg is more toxic to higher organisms, including humans, than inorganic Hg. Hg can affect productivity, reproduction and survival of coastal and marine organisms and the population living near the coast and on islands runs a greater risk of ingesting this highly toxic substance, Kehrig et al. (2006).
In Mytilus species, metals are likely to be absorbed from water and from ingested phytoplankton and other suspended particles and a Me-Hg to total Hg ratio of about 40% in the Mediterranean mussel was reported, Mikac et al. (1996). The soft tissues of all specimens of common mussels from two estuaries in the State of Rio de Janeiro showed percentages of Me-Hg ranging from 31.9% to 64.5%, with an average of 53.2%, Kehrig et al. (2006). These results are similar to other data reported for marine mollusks, Kehrig et al. (2001, 2002) Joiris et al. (2000), Odzäk et al. (2000) and Claisse et al. (2001). Furthermore, a study of Pastor et al. (1994) in which a different suite of metals was measured in the mussel M. galloprovincialis from a polluted area in the western Mediterranean, Spain, showed on average similar total Hg and Me-Hg concentrations.
The digestive gland of the Mediterranean mussel M. galloprovincialis is the preferential organ for the accumulation of Hg, while Me-Hg is mostly accumulated in the soft edible tissue, Boening (2000) and Odzäk et al. (2000).
Mussels showed a higher capacity for the accumulation of Hg compared to other mollusk species, such as oyster and clam, Kehrig et al. (2006). Even though the feeding habits of the mollusks are similar; mussels presented higher Hg and Me-Hg concentrations in their soft tissues than oysters, Kehrig et al. (2006). Filter-feeding bivalves, such as mussels and oysters, accumulate less Me-Hg than fish and hence apparently present a smaller risk to human consumers, Claisse et al. (2001). This is possibly related to their capacity to select particle size and composition of the ingested food they assimilate, and also reflects on the greater ability of mussels to concentrate and excrete Me-Hg and also on their environmental conditions.
The routes of Hg accumulation, including the relative importance of different Hg species, inorganic and organic, and exposure pathways, aqueous vs. dietary, are not yet well understood. Most field studies examined the trophic transfer of Hg by collecting various abiotic compartments, such as water and sediment, and biotic compartments, such as phytoplankton, zooplankton, mussels and fish, to analyze the respective Hg concentrations. On other hand, in estuarine and coastal environments, various environmental factors, including pollutant input, salinity, temperature, and food availability, can vary widely. These external factors are known to influence metal bioaccumulation in organisms by changing either the bioavailability of the dissolved and particulate metals in the water or the physiological attributes of organisms, Suseno et al. (2010).
A recent publication showed that marine organisms might accumulate Hg both by ingestion of contaminated food and direct adsorption from the water column, Wang and Fisher (1996). They can assimilate Hg from ingesting suspended particulate material, but the trace metal assimilation efficiencies depend on the inorganic and organic chemical composition of the particulate material, Gagnon and Fisher (1997). The bioavailability and the chemical species, especially as free ions, influence the toxicity of trace metals and their bioaccumulation by organisms in an estuarine environment. Hg and Me-Hg bioaccumulation is different from that of other metals because the uptake of free metal ions via facilitated transport is not the only important mechanism, suggesting that Hg and Me-Hg accumulation in the presence of large organic compounds occurs through other uptake mechanisms in addition to passive diffusion, Wright and Mason (2000). Dissolved organic matter interacts very strongly with Hg, affecting its speciation, solubility, mobility and toxicity in aquatic ecosystems. DOM reduces the bioavailability of both inorganic and Me-Hg in that the bioaccumulation factors decrease with increasing organic content of the exposure medium, Ravichandran (2004) and Wright and Mason (2000).
4.2.4 Arsenic (As)
As is an element which occurs naturally in seawater and rocks of the Earth, is notoriously poisonous and is commonly used in pesticides, herbicides and insecticides. As in the soil, originating from air emissions in coal-fired power plants, waste recycling, pesticides and treated wood is increasing at a rate to suggest potential public health risks, Luong and Rabkin (2009).
In some areas, the concentration of As in water can attain levels of 1 mg/L, in non-polluted freshwaters it has a concentration lower than 10 μg/L, while in seawater, the concentration ranges from 2.0 to 4.0 μg/L, Devesa et al. (2008). These high concentrations are either due to the presence of As-rich rocks and minerals in aquifers of Taiwan, Bengal, Mexico, Chile, Argentina, Mongolia, Finland, Hungary and the west of the United States, or to anthropogenic contributions, Devesa et al. (2008). In water, As occurs in both inorganic and organic forms, in dissolved and gaseous states. The form of As in water depends on Eh, pH, organic content, suspended solids, dissolved oxygen and other variables. The inorganic forms of As are the most toxic, whereas most organic forms are considered non-toxic, Sloth and Julshamn (2008). Both organic and inorganic As compounds are absorbed almost completely in the gastro-intestinal tract and predominately eliminated from the body via the kidneys as urine, Sloth and Julshamn (2008).
Once As reaches water and soil, its transmission through the food chain is imminent, Suner et al. (1999). It is bioaccumulated by various land and water organisms, although more so by aquatic animals, but there is no evidence of magnification along the aquatic food chain, Suner et al. (1999). As is one of the most toxic elements found and it is present in food in organic or inorganic forms. Additionally, inorganic As(III) salts are more toxic than As(V) salts. The International Agency for Research on Cancer classifies As as a carcinogenic agent for humans – category 1, Sirot et al. (2009).
The levels of As in most foods are very low, with the exception of seafood. Seafood is known to be the most significant source of As in the diet and, consequently, the total human intake of As depends on the quantity of seafood consumed, Suner et al. (1999). As is found in seafood in different chemical forms, differing in their degree of toxicity and the pathologies that they generate, Shiomi (1994). However, the majority of As in seafood is present in the organic, less toxic form, Shiomi (1994). Provided by Munoz et al. (1999), the percentages of inorganic As in seafood are 1–5%, while in bivalve mollusks, they are 1.9–6.5%. Mussels contain a relatively high content of inorganic As compounds, approximately 1–2%, Sloth et al. (2005). The part of inorganic As in foodstuffs has been calculated according to the estimations proposed by the WHO: 75% in meat and dairy products, 65% in poultry and cereals, 10% in fruits and 5% in vegetables, drinking water and other beverages; it was assumed that the As was 100% inorganic, Sirot et al. (2009).
Most of the As accumulated in marine organisms is in the organic, water-soluble form; arsenobetanine which is considered non-hazardous and totally safe for human consumption, Sloth et al. (2003). The ability of marine phytoplankton to accumulate high concentrations of inorganic arsenicals and transform them into methylated arsenicals, which are later efficiently transferred to the food chain, is well documented, Shiomi (1994). The great majority of the As in marine organisms exists as water-soluble and lipid-soluble organoarsenicals that include arsenolipids, arsenosugars, arsenocholine, arsenobetaine, monomethyl arsonate, and demethyl arsinate, as well as other forms, Cao et al. (2009). For most marine species, however, there is general agreement that As exists primarily as AsB, a water soluble organoarsenical that has been identified in the tissues of many marine species, including mussels, Shiomi (1994). The potential risks associated with the consumption of AsB containing seafood seem to be minor: it was neither toxic nor mutagenic, had no effect on metabolic inhibition and showed no synergism or antagonism on the action of other contaminants, it was rapidly absorbed from the gastrointestinal tract and rapidly excreted in urine without metabolism, Sloth et al. (2003, 2005), Sloth and Julshamn (2008).
As does not significantly bioaccumulate in the body, Jones (2007). In humans, arsenate As(V) is first reduced to arsenite As(III), methylated into methylarsonic and dimethylarsinic acids, most of which are than excreted via the renal pathway; excretion via feces, nails and hair is minor, Sirot et al. (2009). The literature results indicate that AsB and As(V) are the dominate species in dry seafood products, while all other As species are present in relatively low concentrations, Cao et al. (2009).
Marine organisms naturally accumulate considerable quantities of organic As compounds, AsB, which are mainly non-toxic, and a very small percentage of inorganic As, arsenite and arsenate, which are very toxic forms. As concentrations in tissues of marine biota show a wide range of values, being the highest in lipids, liver, and muscle tissues, and varying with the age of the organism, geographic location and proximity to anthropogenic activities; in general, tissues with high lipid content contain high levels of As, Eisler (1994).
4.3 The Bioaccumulation of the Toxic Elements in Mussels
Intertidal areas are the natural habitats of marine mussels and they are usually close to estuaries. Therefore, the chance of exposure to many contaminants from land-based activities through the reverine systems as well as sea-based sources is high, and one of its attributes is the possible usage of mussels as a biomonitoring agent for the estimation of pollutant metal concentrations in a sea environment. Among the environmental pollutants, trace metals represent natural constituents in tissues of marine organisms and their basal levels can be affected by marked seasonal fluctuations. Several environmental and biological factors mutually compete to determine such variations, Fattorini et al. (2008). Mussels are sedentary organisms, long-lived, easily identified and sampled, reasonably abundant and available throughout the year, tolerant of natural environmental fluctuations and pollution. Due to their biological and ecological characteristics, mussels have been commonly applied in more than 50 nations during the last 40 years, to provide a time-integrated picture of local contamination, Cantillo (1998).
The importance of bivalves in pollution impact studies is shown by the concept of the International Mussel Watch Program, Goldberg (1975), which has continued to maintain its momentum until today, Rainbow (1995), Sericano (2000) and Kavun et al. (2002). Mussels are well known to accumulate a wide range of metals in their soft tissues. Since it is edible and marketed commercially, the determination of pollutant metals levels in mussel species provides a means of assessing the possible toxicant risk to public health. As pollutant metals are widely distributed in coastal environments, from both natural geological processes and anthropogenic activities, determination of pollutant metals in mussels is important because of their effects on human health, Yap et al. (2004), Sivaperumal et al. (2007), Kljakovic-Gaspic et al. (2007), Turkmen and Ciminli (2007), and these metals are readily accumulated in the soft tissues of the mussel M. galloprovincialis. Some metals, such as Cd and Pb, have long been known to accumulate within the aquatic food chain.
Mussels are nutritional by ensuring the intake of essential minerals, necessary for the maintenance of good health; on the other hand, they can be toxic because certain metals, such as Pb, Cd, As and Hg, are detrimental to health, Szefer (2002) and Sivaperumal et al. (2007). From the toxicological point of view, excessive consumption of metal-contaminated mussel may result in toxicity to humans. Since pollutant metals are inorganic chemicals that are non-biodegradable, cannot be metabolized and do not break down into harmless forms, Kromhout et al. (1985), the measurement of metal levels in the soft tissue of mussels has becoming more significant. Mussels can simply accumulate metals through time, Mubiana and Blust (2007), becoming more and more of a toxic threat as the concentration levels increase. Mussels are used as sentinel organisms and bioindicators to evaluate the toxic effects of chemical pollutants in marine organisms, especially pollutant metals, representing an important tool for biomonitoring environmental pollution in coastal areas. The reliability of mussels as biomonitors of pollutant metal contaminations has been demonstrated by a number of researchers. Levels of metals above the permissible limits would certainly create notorious food image from the public health point of view.
The mussel is a good bioindicator for Cd, Pb, Hg and As, Szefer (2002). The distribution of contaminants in mussel organs is known to vary as a result of the differing affinities of pollutants for binding sites and the different rates of pollutant accumulation in and excretion from tissues, Fernández et al. (2010). It has been reported that metals such as Hg, Cd and Pb accumulate in mussels more rapidly and to a greater extent in the gills than in tissues, such as the mantle, muscle or digestive gland, while the digestive gland and mantle tissues accumulate higher levels of organic pollutants than gills, Fernández et al. (2010). In addition, the spawning season of the mussels and environmental factors may contribute to the wide variability of pollutant metal concentrations in the total soft tissues of mussels, Yap et al. (2006).
4.3.1 The Content Cd, Pb, As and Hg in the Soft Tissues of the Mediterranean Mussel
Several studies demonstrated the presence of significant seasonal and spatial variations of the content of toxic elements in the total soft tissue of the Mediterranean mussels. The Cd, Pb, As and Hg concentrations determined in the soft tissues of Mediterranean mussels, M. galloprovincialis, mainly in last decade all over the world where exist given in Fig. 9.6. and in Tables 9.2–9.6, together with the sites and the years of sampling with the corresponding bibliographical references.
Distribution of the Mediterranean blue mussel over the world: 1. Slovenia, Croatia, Montenegro; 2. Greece; 3. Turkey, Romania; 4. South Korea; 5. China; 6.France; 7. Marocco; 8. Spain, Portugal; 9. California, USA, 10. Italy
Some concentrations were determined over several years and others result from several samples in a single year. Metal concentrations are given in mg/kg dry wt. However, some metal concentrations are given with respect to the fresh weight in the original references, Sunlu (2006), Klaric et al. (2004), Ünlü et al. (2008), Özden et al. (2010). The data from the period 1991 to 2009 are grouped by countries and seas in order to enable the easiest comparison of the concentrations of the toxic metals. Since M. galloprovincialis are aqua cultured and collected from the Mediterranean and Atlantic coast of Spain and France, from Italy- Adriatic and Mediterranean, Adriatic, Greece and in the last 10 years from Turkish coasts, the concentrations of Cd, Pb, Hg and As are primarily compared for these regions, Tables 9.2–9.4.
Some large variations in the Cd, Pb, Hg and As concentrations in M. galloprovincialis from this extensive analyzed region were observed due to the different ages, feeding behaviors and different geographical areas with different natural and anthropological impacts. Important factors which modulate the bioavailability and tissue burden of these pollutant metals include fluctuations of temperature, phytoplanktonic blooms and organic matter, the presence of nutrients, waters fluxes and circulation, up-welling phenomena, freshwater inputs, and also intrinsic species-specific features, such as the phase of reproductive cycle and the associated changes in the relative tissue composition, Fattorini et al. (2008).
Broadly speaking, it can be said that most of the results for the concentrations of pollutant metals, Cd, Pb and Hg, in the investigated mussels were of the same order of magnitude in the case of the Spanish Atlantic and the Mediterranean coast, but significantly higher concentrations were observed in the case of As, especially in Galicia, Cantabria, and the Basque Country, as well as in mussels from Spanish Mediterranean coast, Bartolomé et al. (2010b) and Fernández et al. (2010). The temporal variation had no specific trend and the concentrations were quite constant over a wide range of sites and during time on both sides of the Spanish coastline. The highest mean concentrations were found for As, between 13 and 25.6 mg/kg d.w., in the mussel from both Spanish coastlines, the Atlantic and the Mediterranean. Lower mean concentrations were found for Pb, mainly between 2.0 and 5.0 mg/kg d.w., and Cd, between 0.4 and 2.0 mg/kg d.w., and the lowest were found for Hg, between 0.05 and 0.35 mg/g d.w, Bartolomé et al. (2010b) and Fernández et al. (2010).
Significant downward trends were observed for the concentrations of Pb and Hg in mussels from a large number of sampling stations along the coast of Spain, while the Cd concentrations in the mussels showed upward trends Benedicto et al. (2003). The mean concentrations of Pb in mussels were lower than those determined in previous studies that were performed in the same area. The distribution of Pb in a marine environment is controlled by atmospheric deposition; the concentration of excess Pb in marine organisms is directly linked to human activities, Besada et al. (2002). A study of the spatial distribution of chemical contaminants realized using mussels allowed the identification of clear hot spots along the Spanish coastline, Fattorini et al. (2008).
Along the French Mediterranean coast, the Cd concentrations were in the same order of magnitude as in the open sea and in lagoons (mean value: 1.1 mg/kg), with the exception of one lagoon with concentrations of up to 4.5 mg/kg. The Hg background level was stable and below 0.1 mg/kg with high levels in some lagoons (0.15 mg/kg), Andral et al. (2004). High concentrations of Hg were also observed in the mussels of Toulon waters (0.25 mg/kg). The Pb background level was 1.13 mg/kg, with extreme values in one lagoon (4.86 mg/kg) and in the coastal waters of large urban areas (3.5 mg/kg), but the mean As value was 20 mg/kg, Andral et al. (2004). It is oblivious that the concentrations of As, Pb, Cd and Hg in M. galloprovincialis from the Mediterranean part of Spain were higher on average than those in the mussels from the Mediterranean coast of France. However, the mussels along the Spanish Mediterranean coast were collected in May–June 2003, in the pre-spawning period, Fernández et al. (2010), while those from the French Mediterranean coast after the spawning period, in July 2000, Andral et al. (2004). In the case of Atlantic coast, the mussels from Spanish and French waters contained similar concentrations of these metals, Table 9.2. It is interesting to note that the mean concentrations of As, Cd and Hg were generally higher in mussels from the Mediterranean coast, but the Pb concentration was lower than in the mussels from the Atlantic coast. Exceptions were mussels from some “hot spots” on the Mediterranean coast, in which very high concentrations of Pb were found, whether they were from the French or Spanish coast, 83.2 and 57.83 mg/kg d.w., respectively. The overall trends observed along the French coasts for 1979–1999 confirmed decreasing values for Cd and Pb, while for Hg the local decreases were about twice, Regoli (1998) and Fattorini et al. (2008). In both cases, on the French and Spanish coastal areas, the pollutant metal concentrations in the mussel M. galloprovincialis were in the order: As > Pb > Cd > Hg.
In Tables 9.2–9.4, the results for the pollutant metal concentrations in the whole edible soft tissues of mussels from the Spanish and French regions are also compared with the results of studies from different locations of the Mediterranean Sea, such as Italian, Hellenic and Turkish coastal regions, since they are producers of this mussel. The mean concentration of Pb in mussels from the Ionian Sea, Italy, was higher than in mussels from the Tyrrhenian Sea in Italy, but the opposite was true for the Cd concentrations, Cardellicchio et al. (2008), Lafabrie et al. (2007). In the last decade, the Cd, Pb and Hg concentrations were much lower than in previous studies realized with mussels from the Tyrrhenian Sea, Capeli et al. (1978). For Pb, this decrease could be the result of a decrease of the Pb concentrations in gasoline. In the early 1970s, very high Hg concentrations were observed in some coastal areas, in ‘hot spots’, near harbors and industrial areas, Mikac and Picer (1985). Results from the northern Adriatic Sea in Italy showed higher levels of Cd, Pb, Locatelli (2003), and As, Giusti and Zhang (2002), when compared with studies from the Ionian Sea and Tyrrhenian Sea, Lafabrie et al. (2007) and Cardellicchio et al. (2008). Mussels from the Italian Adriatic coast have higher Cd and Pb levels, 3.7–4.3 and 15.8–29.0 mg/kg d.w, respectively, than mussels from the eastern part of the Adriatic Sea, 0.4–2.4 and 0.9–15.1 mg/kg d.w, respectively, at hot spots. The highest concentrations of As, Pb and Cd in mussels from the northern Adriatic Sea are correlated to the industrial development of the Venetian region over the last 20 years and the impact of the River Po, Licata et al. (2004). From 1986 to 2003, the Italian National Mussel Watch showed national decreasing trends of the Cd concentrations in mussels, but other trace metals exhibited only local or regional variations with trends in the concentrations in bivalves more or less evenly split between increases and decreases, Fattorini et al. (2008).
Quite limited data are available for the As concentrations in Mediterranean mussels, normally obtained in specific periods or in different seasons of a single year. The results obtained in these investigations generally indicated higher values of As in Adriatic mussels, Stankovic et al. (2006, 2008) and Jovic et al. (2011), than in organisms from unpolluted sites of the French and Spanish Mediterranean coast, Andral et al. (2004) and Fernández et al. (2010), and the Tyrrhenian coasts, Fattorini et al. (2008), Bartolomé et al. (2010a,b) and Fernández et al. (2010), except two hot spot locations with 82.6 and 60.0 mg/kg d.w. levels of As on the Mediterranean Spanish and French coast, respectively. Overall, these results confirm the general distribution of As compounds in mussels which, with a few exceptions, tend to exhibit their basal content of this element mostly as organic, non-toxic molecules. Factors controlling the bioavailability of this element in the marine environment are complex to recognize and may include, e.g., redox conditions, iron and manganese oxides, acid-volatile sapphires and total organic carbon, Fattorini et al. (2008).
Basal levels of trace elements in mussel can also exhibit geographical differences, such as those related to site-specific geological or environmental features. Well known examples include the Hg anomaly in the Tyrrhenian Sea, which is responsible for the elevated bioavailability of this element, Fattorini et al. (2008). The total Hg values in the Mediterranean and the Marmara Sea (Bosphorus) species were generally higher than those found in the Atlantic, Tables 9.2–9.4. The levels Hg in mussel from the French and Spanish Mediterranean coast, including hot spots, are in the range 0.02–1.24 and 0.03–2.21 mg/kg d.w., respectively, while in the Atlantic and Adriatic Sea, they are in the range 0.01–0.88 and 0.02–0.32 mg/kg d.w, respectively. Only on the eastern Adriatic coast, there were two hot spots with high levels of Hg in the mussels: 8.58 and 1.06 mg/kg d.w., in Croatia, Kastela Bay, and in Montenegro the harbor Bar, respectively, Kljakovic-Gaspic et al. (2006a) and Stankovic et al. (2008), Jovic et al. (2010). In the Marmara Sea, M. galloprovincialis from Bosphorus Asian and European side had very high levels of Hg: 1.03–2.94 and 0.14–2.86 mg/kg, Kayhan (2007). The higher Hg levels are deemed to be the result of the region being in the Mediterranean – Himalayan mercuriferous belt, Shoham-Frider et al. (2002).
The highest measured As levels are in the mussel from the Adriatic and Aegean Sea, Fattorini et al. (2008), Orescanin et al. (2006), Stankovic et al. (2006), Jovic et al. (2010) and Schaeffer et al. (2005), Table 9.2. It was the lowest in the mussel from the Marmara and Black Sea, Özden et al. (2010) and Ergul et al. (2007). The high level of As in the mussels of the eastern Adriatic could be explain by the exhibited high concentrations of As (1–19 mg/kg) found in the sediments of the southern Adriatic, Dolenc et al. (1998). A better knowledge of the natural variability of the concentrations of trace metals in mussels from the Adriatic Sea is of special interest due to the different geographical characteristics and human activities which could have an impact on this basin and the relative lack of appropriate reference values available for pollutant metals, which are required when monitoring various anthropogenic pressures, i.e., dredging operations, coastal management and off-shore activities to cite just a few, Fattorini et al. (2008).
The Mediterranean Mussel Watch program suggests a dominant source of metal contamination from urban and industrial activities and less important inputs from continental and agricultural origins, Sunlu (2006). The levels of trace metal concentrations in the soft tissues of mussels indicate that the inner part of the Izmir Bay is the most contaminated area along the Turkish Aegean Sea coast. Traffic is very important along the Turkish Aegean Sea coast and it could be a major source of Pb pollution of the coastal seawater. Location is the primary factor along the Turkish Aegean Sea coast and metal levels vary only depending on the location. There is no indication of a seasonal variation in the metal levels, Sunlu (2006). Consequently, hot spot areas are especially near large urban and industrial centers, notably the Izmir and Candarli Bay. However, localities relatively far from anthropogenic sources, e.g., the Sigacik and Gulluk Bay, have a considerably high potential for aquaculture, since they are affected very little by pollutant metal contamination, Sunlu (2006). Cd and Pb are considerably lower compared with the values obtained in large-scale research into the pollutant metal levels in mussels on the Atlantic coast and in countries around the Mediterranean Sea, Tables 9.2–9.4.
If the data of pollutant metals in mussels from the Turkish seas are analyzed, the highest levels of Cd and Hg were found in mussels from the Bosphorus, Kayhan et al. (2007). Concentrations of Cd in the soft tissue of M. galloprovincialis from the Bosphorus were high and in general displayed significant variation from station to station, Kayhan et al. (2007). From Bosphorus European and Asian side, there were very high concentrations of Cd up to 8.95–10.68 mg/kg d.w, Kayhan et al. (2007), which are similar to the Cd levels in mussels from the French Atlantic coast, up to 11.70 mg/kg d.w., Deudero et al. (2007). Along the Turkish coastline, the highest Pb concentrations were found in mussels from the eastern Black Sea, up to 22.0 mg/kg, Çevik et al. (2008).
From Tables 9.2–9.4, it could be concluded that the highest concentrations of Cd and Pb were found in mussels from hot spots on the French and Spanish Mediterranean coast, up to 36.2 mg/kg d.w. and 83.2 mg/kg d.w., respectively. Mussels from the Adriatic Sea, Croatia, had the highest concentrations of Hg, up to 8.58 mg/kg d.w, than mussels from the Atlantic coast, Mediterranean and Black Sea, but again at hot spots. Generally, the levels of Cd, Pb and Hg were the lowest in mussels from the Aegean Sea, compared to the others investigated seas, Tsangaris et al. (2004) and Catsiki et al. (2004), but a very high level of As was found, Schaeffer et al. (2005). Generally, Hg was present in low concentrations; higher average Hg levels were observed in M. galloprovincialis from the Marmara Sea, Bosphorous, Kayhan et al. (2007), but the results for As indicated that a large proportion of As was in the organic form, Marcotrigiano and Storelli (2003). In Mediterranean mussel from the all investigates Seas, the concentrations of these pollutant metals were in the following order: As > Pb > Cd > Hg.
Despite the considerable seasonal and inter-annual variations, data on trace metal concentrations presented in this work are generally within the range of mean values more recently reported for Mediterranean mussels sampled or translocated in unpolluted sites of the French coast, Andral et al. (2004), the NW Mediterranean, Roméo et al. (2003a), the Spanish Mediterranean coast, Benedicto et al. (2003), the North Tyrrhenian Sea, Nigro et al. (2006), the North Aegean Sea, Catsiki and Florou (2006), the Turkish Aegean Sea, Sunlu (2006), the Black Sea, Çevik et al. (2008) and the Croatian coast, Kljakovic-Gaspic et al. (2007), if the hot spots would be excluded. Most of the examined metals showed a seasonal decrease in July and the highest values in February and April. A similar seasonal trend was described by other authors, Nesto et al. (2007). Bioaccumulation values were generally much lower than the threshold metal limits established for mollusk consumption by the EC (2006), Table 9.1, and were generally similar to previous values obtained for the same species sampled at various sites, Nesto et al. (2007), Fattorini et al. (2008), Vidal-Linan et al. (2010), Desideri et al. (2010).
4.4 Dietary Exposure Assessment
It is well-known that the intake of food contaminated with chemicals can lead to intoxication episodes that can be described as acute or, when the disease appears after a latent period of time, chronic. The chemicals producing the latter tend to accumulate in the body during long periods of time, producing illness when the levels reach critical values in certain tissues. Ingestion of contaminated food is the principal way of human exposure to these compounds, accounting for >90%, if compared to other ways, such as inhalation and dermal contact. Due to their persistence and lipophilic character, they tend to concentrate in the food chain and are particularly associated with fat, foodstuffs of animal origin being one of the main sources, Bordajandi et al. (2004).
The consumption of fish and fishery products in the European Union countries, such as France (29.7 kg year–1 per capita), Germany (12.2 kg year−1 per capita), Greece (22.7 kg year−1 per capita), Italy (23.1 kg year−1 per capita), Portugal (57.4 kg year–1 per capita), Norway (50.0 kg year–1 per capita) and Poland (9.6 kg year−1 per capita), is still low, Kwoczek et al. (2006). As there is no data on the average national Rate of Shellfish Consumption, the Provisional Tolerable Weekly Intake and the Tolerable Daily Intake were employed as standards for calculating the metal concentration levels of concern associated with mussel consumption. According to FAO/WHO (2004), PTWI is defined as μg of metal per kg of body weight, μg/kg body weight/week, or mg of metal per adult, where an adult is assumed to weigh 60 kg. According to the FAO/WHO, the average weekly intake for adults was estimated to be 1.5 mg for Pb (PTWI Pb = 25 μg/kg body weight/week), 0.42 mg for Cd (PTWI Cd = 7 μg/kg body weight/week), 0.9 mg for As (PTWI As = 15 μg/kg body weight/week) and 0.3 mg for Hg (PTWI Hg = 5 μg/kg body weight/week) The PTWI for Me-Hg was set at 1.6 μg/kg of body wt/week. In this study, a consumption rate of 28.6 g/person/day was used to calculate the level of concern for the low mussel consumption group, assumed by taking 200 g/person/week as the one mussel meal, to calculate the Tolerable Daily Intake (μg/person/day) for the each element, Table 9.7.
In this study, the environmental health risk was assessed by a comparison between the environmental status, as represented by the concentrations of the metals in mussels, and threshold values likely to cause adverse effects in human consumers. In this context, a risk quotient can be calculated as follows:
The Risk Quotient was calculated as the ratio between the concentration of a trace metal in the mussels and the level of concern for that metal, Fung et al. (2004), Kljakovic-Gaspic et al. (2007). The Level of Concern is the “threshold concentration” of a metal above which a hazard to human health may exist, and it can be calculated as follows:
Results of the evaluation of the risks to human health associated with the consumption of Mediterranean mussel containing pollutant metals are summarized in Table 9.8. The Risk Quotient was calculated for the best, median and worst-case scenario, RQ bcs, RQ mcs and RQ wcs, respectively. In the present case, Risk Quotient for the best scenario was calculated for the minimum concentrations, Risk Quotient for the median and RQ wcs for the maximum concentrations of the metals (mg/kg wet weight) found in the investigated mussels to estimate the potential exposure levels of humans related to mussel consumption. For cases where RQ < 1, the chemicals involved are unlikely to cause harm to human consumers, Fung et al. (2004), Kljakovic-Gaspic et al. (2007).
The concentration ranges and median of pollutant metals present in the Mediterranean mussel were converted into the wet weight, Yap et al. (2004) and Kwoczek et al. (2006) and used to estimate the potential exposure levels of pollutant metals related to the consumption of mussels, Table 9.8. It is noteworthy that the RQ wcs values were higher than one for As (Mediterranean Sea, Adriatic Sea and Atlantic coast), for Cd and Pb (Mediterranean Sea) and Hg (Adriatic Sea) suggesting that probable health associated problems might be encountered in pollutant shellfish consumers. It is related to mussels from hot spots, such as urban areas, near the mouth of rivers, harbors and lagoons. Of particular concern were the Cd, Pb and As concentrations in mussels from the hot spots in the Mediterranean Sea because the values of RQ wcs were 3.45, 2.22 and 3.67, respectively, Table 9.8. The risk quotients in the best case scenario, RQ bcs, for Cd, Pb, Hg and As indicated that these metals are probably not of great health concern for mussels consumers, Table 9.8. The RQ mcs values for As for consumers of mussel from the Mediterranean Sea, Atlantic coast and Adriatic Sea indicate that this metal could be of health concern, but it should be noted that the As present in mussels is mostly in the organic form, which is relatively non-toxic to humans and readily excreted.
Thus, As is unlikely to represent a significant risk to human health, since in the mussels, the maximum level of the more toxic, inorganic form of As is less than 5%, Sloth et al. (2005). Overall, the assessment indicates that metals may pose a health risk to pollutant seafood consumers, especially related to the levels of Pb and Cd in mussels from hot spots. In the case of the risk quotient values for Hg, it should be born in mind that the toxic Me-Hg in mussels participates by about 40–50% to the total Hg. All the risk quotient values for As and Hg in this study were calculated related to the total concentrations of Hg and As.
It should be emphasized that the consumption data used in this study are based on one meal of 200 g of Mediterranean mussel per week. As seafood, and particularly mussels, consumption rates can vary greatly between countries and among specific sections of a community; these standards should only be used for screening purposes. For example, if the consumption of two 200 g meals of the mussels per week is considered, the risk quotient values would be two times higher but related to the health of mussels consumers, the pollutant metals would still not be a health concern for the consumers of M. galloprovincialis, excluding the mussels with maximum concentrations found or with RQ wcs >1 from the hot spots. Generally, if the consumption of mussels from hot spots is excluded, it is safe to consume Mediterranean mussel.
The PTWI values appear to support the conclusion that risk to human health from dietary exposure to pollutant metals from mussels is relatively low. Based on typical Cd concentrations of 0.7 and 0.1 mg/kg in Italy and France, respectively, a 70 kg adult would need to consume ≈1.0 kg and ≈7.0 kg of mussel flesh per week to exceed the PTWI value in Italy and France, respectively, Falcó et al. (2006). Dietary intake of mussels must be even larger than 7.0 kg to exceed the PTWI values for the other pollutant metals tested. However, the calculations are based on the current PTWI values and it is unknown whether these are sufficient to mitigate lifelong dietary exposure to pollutant metals, Falcó et al. (2006). Permissible values change over time, a value that is assumed to be innocuous at present may be considered dangerous in the future. For this reason, values below the current PTWI values should not automatically be considered ‘low-risk’ to consumers and values that are close to the current limits should be taken seriously. In addition, individual susceptibility to toxins in humans is variable, meaning that even concentrations below the current ‘permissible’ values may lead to toxic effects in people with high sensitivity. Consequently, it is hard to assess the human health impacts of exposure to pollutant metals through diet. For some people with a low dietary tolerance, the metals might result in toxic effects. For example, especially Maori with a low dietary tolerance, increase their risk of toxic effects because of a higher consumption of shellfish than the general public, Whyte et al. (2009).
Further information on the type, amount and frequency of shellfish consumption is required to adequately assess the possible health risk associated with pollutant metals ingestion. The intake of As, Cd, Hg and Pb in Spain from the consumption of 14 marine species, including shellfish and fish, were estimated and the PTWI for most of the population was within acceptable limits, although the Me-Hg concentrations for boys were excessive, Falcó et al. (2006). This study highlights the particular risk of pollutant metal accumulation in children who, because of their smaller body weight, require less seafood to exceed regulatory limits. Consumption of Cd and As contaminated seafood was found to pose a potential health risk to fisherman in Taiwan, Whyte et al. (2009), again highlighting the increased risk of pollutant metal accumulation in sectors of the population that consume more seafood than ‘average’, Whyte et al. (2009).
To prevent health risk from the pollutant metals exposure, the European Commission, EC (2006), Das et al. (2009), established in the past years maximum levels permitted in seafood and recently proposed target and action plans in order to reduce their presence in different food items. People consuming large amounts of contaminated seafood may have elevated concentrations of pollutants in their tissues compared to the general population, Han et al. (2000).
Comparison of the published data with European legislation, Table 9.1, showed that the levels of Cd, Pb and Hg usually did not exceed the existing limits in all the mussels analyzed, excluding mussels from hot spots such as lagoons and harbors, Andral et al. (2004), Nesto et al. (2007) and Jovic et al. (2010). In EC (2006), the Maximum Permissible Limits in edible tissues of mussels are 0.5 mg/kg for Hg, 1 mg/kg for Cd and 1.5 mg/kg for Pb related to fresh weight, Nesto et al. (2007), Amiard et al. (2008), Das et al. (2009). Contaminants in mussels were examined from the standpoint of food safety in the Mediterranean and Black Sea basins. In mussels from some locations, the levels of Pb and Cd exceeded the health standards, i.e., mussels from the Adriatic Sea, Giusti and Zhang (2002) and Kljakovic-Gaspic et al. (2007), but in mussels from the Taranto Gulf (Ionian Sea, Southern Italy), the Pb and Cd concentrations were always below the levels recommended by the European Community, Cardellicchio et al. (2008). Concentrations found for Cd and Pb indicate that the mollusk populations under investigation pose no health risk to seafood consumers, because their metal contents were within the permissible range established for safe human consumption, Cardellicchio et al. (2008).
The mean concentrations of pollutant metals determined in the mussel M. galloprovincialis from Istanbul fish markets and the eastern Black Sea showed that the contents of Cd and Pb were below the MPL for fish proposed by EC (2006) and the Turkish Food Codex from 2002, Ozden et al. (2010). The levels of Hg and As were found to be above the MPL in mussels from the eastern Black Sea, Cevik et al. 2008; Ozden et al. (2010) and Das et al. (2009). Mussels from the Marmara Sea are safe regarding the Cd and Hg concentrations but may contain Pb above the permissible limits, Mol and Alakavuk (2010). The levels of trace metal concentrations in the soft tissues of mussels indicate that the inner part of the Izmir Bay is the most contaminated area along the Turkish Aegean Sea coast. The levels of the pollutant metals in M. galloprovincialis from the North Aegean Sea are characterized, in general, as being below the MPL values and comparable to those from other non-polluted Mediterranean areas, Catsiki and Florou (2006).
4.5 Impact of Mussel Consumption to Human Health
4.5.1 Beneficial Effects If Mussel Consumption
By 2002, fish fisheries and aquaculture products contributed 12% to the total protein for human consumption, although there are no detailed global statistics on the provision of other essential minerals and components, FAO (2006). The total content of minerals in raw marine fish and invertebrates is in the range of 0.6–1.5% wet weight, Ozden et al. (2010). An epidemiological study in Japan showed that seafood was the largest source of vitamin B6 (16–23% of the total intake) and B12 (77–84%) in the diet, Yoshino et al. (2005). Many species of fish and shellfish are rich sources of Omega 3 fatty acids, Ackman et al. (2000) and the health benefits associated with the consumption of seafood products are particularly important for the prevention of heart-related diseases and for many vulnerable groups, such as infants and children, and pregnant and lactating women, Cozzolino et al. (2001), Christophoridis et al. (2009) and the positive impact of seafood consumption on bone mineral density has also been reported, Zalloua et al. (2007). Meeting nutritional requirements of antioxidants, particularly Zn, to defend human beings against xenobiotic-induced oxidative stress and associated toxic hepatitis could be improved through zinc-rich seafood consumption, Stehbens (2003).
In M. galloprovincialis, proteins contribute about 60% to the dry weight of the soft tissues, Karaycel et al. (2003). Mussels are very important for marine ecology and for the human diet, since they are a cheap source of protein for human consumption, Yap et al. (2004), Amiard et al. (2008). Consumption of these bivalve mollusks provides an inexpensive source of protein of a high biological value, essential minerals and vitamins, Fuentes et al. (2009), Ozden et al. (2010). From the nutritional point of view, mussel is an important food source for supplying essential elements, e.g., Ca and Fe, and also certain vitamins, such as niacin, thiamine and riboflavin, Yap et al. (2004), Amiard et al. (2008). Minerals and trace elements are very important components in human diets as both their deficiency and excess may cause serious health problems. Trace metals can be divided into essential elements and non essential elements. The effects of deficiency of essential trace elements are the most severe during development and growth and they are especially important for infants and children, Cozzolino et al. (2001).
4.5.2 Risks of Mussel Consumption
On the other hand, the toxicity effect of pollutant metals in living marine organisms was recognized as early as the early decades of the twentieth century, although it received little attention in the past. This effect was considered of secondary importance. However, all metals are potential toxins at some concentration and the non-essential elements, e.g., Hg, Pb, Cd and As, are particularly toxic at relatively low concentrations, Bat et al. (1999), Çevik et al. (2008). Lately, however, there was a growing concern regarding toxic contaminants, in general, and toxic pollutant metals in seawater, in particular. This awareness occurred in the wake of the tragic events of the Minamata and Itai-itai Hg and Cd poisoning cases, respectively, which erupted in Japan around the middle of the twentieth century, Fleming et al. (2006) and Malik et al. (2010). Ever since, the disease caused by poisoning human beings with Hg-contaminated seafood was named Minamata after the Japanese Bay where it was first recognized and the name itai-itai was given to the disease caused by poisoning humans with seafood contaminated with Cd, Fleming et al. (2006) and Malik et al. (2010).
In Minamata Bay, the Hg had come from industrial discharges into the bay. Eating fish that had accumulated Hg in Minimata Village between the years 1953 and 1960 poisoned hundreds of individuals. Soon after this tragedy, the other Itai-itai tragedy erupted, also in Japan, when eating fish contaminated with Cd metal this time, poisoned a lot more humans. The disease was named after the characteristic screams, known as the itai screams, which was a cry common to all poisoned casualties. These tragic Japanese incidents flared a vivid awareness of the problem of bioaccumulation of metals by marine organisms and spurred research on the fate and impact of metals in marine environments and their negative effects on human health.
Seafood products in general also pose carcinogenic and other adverse effects on human health due to biomagnifications over time. For example, cancer and damage to the nervous system, etc. have all been documented in human beings as a result of metal consumption.
Many pollutant metals accumulated in mussels can also be accumulated in the food chain. These non-essential elements, such as Cd, Pb, Hg and As, are non-biodegradable chemicals which do not have any positive effects on organisms and are harmful already at low doses. They cannot be metabolized into harmless forms and accumulate with time in the human body and might act alone or together over time to cause the disease, as well as other health problems. Thus, people consuming mussels could be exposed to these potentially dangerous to health metals, Han et al. (2000), Giusti and Zhang (2002), Clarkson (2002), Yap et al. (2004), Kwoczek et al. (2006), Kljakovic-Gaspic et al. (2006b), Türkmen and Ciminli (2007), Sivaperumal et al. (2007), Çevik et al. (2008).
Cd, a metal with high toxic effects, which is strongly bioaccumulated in mussels, has an elimination half-life of 10–30 years and accumulates in the human body, particularly the kidney, Amiard, et al. (2008). Cd may act as an acute and chronic type of poison. In chronic exposure, the first sign is kidney damage, usually diagnosed by increased excretion of low molecular weight proteins, Widmeyer et al. (2004). Over time, Cd can accelerate osteoporotic process, since a high calcium dose can inhibit Cd absorption. The reverse situation – the inhibition of calcium absorption by Cd – has also been reported. This interaction is of special importance because of the suggested role of Cd in the development of bone softening due to decalcification, a characteristic of ltai-itai disease, Han et al. (2000).
Absorbed Pb is bound to erythrocytes in the blood and initially distributed to the liver, kidney and heart, where it preferentially binds to cell membranes and mitochondria, Widmeyer et al. (2004). Most forms of Pb are then distributed and stored in the bones. The primary root of elimination is via the feces (90%) and the remaining via the urine (10%), Gilbert (2004). Pb is known to cause both acute and chronic adverse effects in the hematopoietic, nervous, gastrointestinal and renal systems, Widmeyer et al. (2004). Acute poisoning causes gastrointestinal colic, often resulting in mortality, while chronic poisoning causes anemia due to a decrease in the hemoglobin levels leading to organ damage in one or all of the four above-mentioned systems, Gilbert (2004), but Pb is not-carcinogenic, Chang (1996).
Hg is highly toxic and extremely damaging to cellular and tissue function, Crinnion (2000) and Fleisher (2001). Hg exposure reduces the mucosal entry of sugars and amino acids to 80–90% of the control levels in the small intestine cells within several minutes and blocks intestinal nutrient transport by interacting directly with the brush border membrane transport proteins. Both Me-Hg and elemental Hg, once absorbed, can cross the blood-brain and placental barriers, Crinnion (2000) and Fleisher (2001). Both forms of Hg are immunotoxic, although they differ quantitatively and qualitatively in their effects on the immune system. Me-Hg accumulates mainly in the kidneys, liver, and brain, Fleisher (2001). Elemental Hg may accumulate in the brain, lungs, fatty tissues, kidney, liver and digestive tract. Over time, Hg accumulates and is slowly converted into inorganic Hg, Crinnion (2000). As inorganic Hg, it binds to sulfur-containing molecules, such as hemoglobin in the blood and the powerful antioxidant glutathione, thus depleting their levels. The increased danger associated with Me-Hg is that it can also have a direct effect on cells without being converted into the inorganic Hg form. Both forms of Hg affect the following systems: nervous system, cardiovascular system, immune system and reproductive system, Crinnion (2000) and Fleisher (2001).
Hg is highly toxic and extremely damaging to cellular and tissue function. It is important that everyone but especially those most at risk, such as pregnant women, is aware of the Hg toxicity of fish. Fetal development is the most dangerous time for Hg toxicity.
The effects of As, mainly caused by inorganic As, may produce inhibition of growth, skin discoloration, respiratory problems or even death, Eisler (1994). Illnesses associated with excessive inorganic As intake include skin, lung and heart conditions, gastrointestinal diseases and possible carcinogenic effects. As(III) compounds are bound by red blood cells and affect the activity of many enzymes, particularly those involved in the respiratory process, Eisler (1994). There are a number of potential mechanisms by which As affects tissues that might lead to cell death, but intracellular calcium or enzyme systems regulated by calcium may alter the toxicity of arsenate, Luong and Rabkin (2009). Organic As neither causes cancer, nor is it thought to damage DNA, but exposure to high doses may result in nerve injury and stomach problems, Eisler (1994).
It is emphasized in the literature that the metabolism and toxicity of As vary greatly between species, and that the effects are significantly altered by numerous physical, chemical, and biological modifiers. Adverse health effects, for example, may involve the respiratory, gastrointestinal, cardiovascular, and hematopoietic systems, and may range from reversible effects to cancer and death, depending partly on the physical and chemical forms, Luong and Rabkin (2009).
Since pollutant metals are non-biodegradable inorganic chemicals which cannot be metabolized and do not break down into harmless forms, Kromhout et al. (1985), the measurement of their concentration in mussel soft tissue has become increasingly significant. Accumulation of toxic metals to above permissible limits in M. galloprovincialis would certainly create a notorious food image from the public health point of view, as it is well known that chronic exposure to pollutant metals, such as Cu, Pb and Zn, is associated with Parkinson’s disease and the metals might act alone or together over time to cause the disease, as well as other health problems, Gorell et al. (1997). Zn appears to have a protective effect against the toxicities of Cd and Pb and its toxicity is rare, Sivaperumal et al. (2007). As(V) causes damage to the heart and blood vessels cells, Luong and Rabkin (2009). A link between traditional food sources high in Cd and diabetes has been postulated in Australian Aborigines, Satarug et al. (2003), and high Cd concentrations have also been associated with prostate cancer, Vinceti et al. (2007), while high Hg and low Zn concentrations have been linked to autism, Yorbik et al. (2004). Although previous studies found a link between shellfish consumption and protection from certain diseases, e.g., myocardial infarction, Yuan et al. (2001), the relative risks and benefits of seafood consumption are hard to assess Whyte et al. (2009) and Yuan et al. (2001).
5 Conclusion
Mussel production and consumption has been increasing worldwide. There is a growing demand for bivalves, not only in historically developed countries, but also in developing regions. The prospects for expansion of the bivalve industry in developing countries will depend on their ability to build reliable monitoring and inspection programs and implement sustainable farming practices. The global outlook suggests a need for a 50% increase in world food production within next 30–40 years. This is a tremendous challenge in itself, also bearing in mind that food production is a key driver in the degradation of the environment and natural resources.
The metal load is higher in inshore waters and, consequently, in the mussels inhabiting them, owing to the elevated levels of elements in the coastal zone. Mussels as filter feeders accumulate trace metals from food, from suspended matter, or directly from seawater, whether or not these metals are essential to their metabolism. Mussels may even take up certain metals to a level above that in the surrounding waters; hence the degree to which they are accumulated is very much species-specific.
For monitoring programs, in which the Mediterranean mussels are used as bioindicator organisms, some criteria should be adopted in the mussel sampling phase. Mussels should be taken in the same period and at the end of the reproductive cycle, when the percentage of metal concentration obtains its highest value, late winter. Otherwise, comparisons between mussels at different stages of the reproductive cycle would show different concentrations of metals, which could simply be a function of the seasonality in the reproductive cycle. Furthermore, mussels should be of the same size and be sampled from the same depth. Only by following these instructions is it possible to obtain, in different geographical areas, homogeneous data that can be easily compared to each other.
The highest producers of cultivated M. galloprovincialis as seafood are Spain, Italy, France, Greece and Turkey. The levels of pollutant metals in the mussel from these countries depend upon the geographical region, hydrological impact and the period of sampling. Levels of Pb, Cd, Hg and As in the Mediterranean mussel are of the same order of magnitude in the Atlantic, Mediterranean, the Adriatic, Aegean and Black Sea regions. The highest values of pollutant metals in M. galloprovincials were in the hot spots of the urban areas, near the mouth of rivers, harbors and lagoons of the Mediterranean and Atlantic coast, such as in the Bosphorus European and Asian side and the Izmir Bay in the Aegean Sea. If the mussels from the hot spots are excluded, in this whole native region of M. galloprovincials, all the investigated metals were not of great health concern, including As, which is present in mussels mostly in the organic form, which is not toxic to humans.
As the Black Sea and the Mediterranean Basin will potentially be the largest producers of the Mediterranean mussels in the future, health of the mussels consumers will depend on integrated management of the land and near-shore components of the coastal zone. Human health impacts caused by the consumption of contaminated seafood were nearly always related to the quality of the environment where the aquaculture products were produced. For this reason, it is important to provide sustainable management of shellfish harvesting waters and, simultaneously, maintain public health. The production and management of cultivated mussels also require integrated work between health, environmental and food regulators and the commercial and casual exploiters of mussel resources.
Abbreviations
- AQ:
-
Aquaculture
- AsB:
-
Arsenobetanine
- BC:
-
Before Christ
- CIESM:
-
Commission Internationale pour l’Exploration Scientifique de la Mer Mediterranee
- CLOC:
-
Consumption Level of Concern
- DOM:
-
Dissolved Organic Matter
- d.w.:
-
Dry weight
- EC:
-
European Commission
- EEC:
-
European Economic Community
- Eh:
-
Soil Redox potential
- EQS:
-
Environmental Quality Standards
- EU:
-
European Union
- FAO:
-
Food and Agriculture Organization of the United Nations
- FSANZ:
-
Food Standards, Australia New Zealand
- iAs:
-
inorganic Arsenic
- LOC:
-
Level of Concern
- Me-Hg:
-
Methylmercury
- MED POL:
-
Marine pollution assessment and control component of MAP
- MMW:
-
Mediterranean Mussel Watch
- MPHT:
-
Ministry of Public Health Thailand
- NW:
-
Northwest
- PTWI:
-
Provisional Tolerable Weekly Intake
- RINBIO:
-
Biological Network Integrators, Réseau Intégrateur Biologique
- RNO:
-
National Network for the Observation of Marine Environment Quality, French Mussel Watch
- RQ:
-
Risk Quotient
- RQbcs :
-
Risk Quotient for the best scenario
- RQmcs :
-
Risk Quotient for the median scenario
- RQwcs :
-
Risk Quotient for the worst case scenario
- RSC:
-
Rate of Shellfish Consumption
- t:
-
Tonne
- TDI:
-
Tolerable Daily Intake
- t y−1 :
-
Tonne per year
- UK:
-
United Kingdom
- UNEP/MAP:
-
United Nations Environment Programme/Mediterranean Action Plan
- USA, US:
-
United States of America, United States
- USFDA:
-
Food and Drug Administration of the United States
- WB:
-
Weight Basis
- WHO:
-
World Health Organization
- WMW:
-
World Mussel Watch
- wt:
-
Weight
- w.w.:
-
Wet weight
- y:
-
Year
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Stankovic, S., Jovic, M., Stankovic, A.R., Katsikas, L. (2012). Heavy Metals in Seafood Mussels. Risks for Human Health. In: Lichtfouse, E., Schwarzbauer, J., Robert, D. (eds) Environmental Chemistry for a Sustainable World. Environmental Chemistry for a Sustainable World. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2442-6_9
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